Vigna nakashimae is a wild species closely related to the azuki bean (V. angularis), with salt-tolerance abilities. The present study aimed to explore the genetic and salt tolerance diversity within the species, by evaluating the phylogenetic relationships of 55 accessions of V. nakashimae including 25 newly collected from the Gotō Islands and Iki in Nagasaki Prefecture, Japan. We conducted salt-tolerance analysis for 48 of the accessions, including 18 of the newly collected accessions. Phylogenetic analysis based on single-nucleotide polymorphisms obtained from MIGseq and RADseq analyses revealed the genetic diversity of V. nakashimae to reflect the geographic arrangement of the habitat islands. Korean accessions formed one clade, while Japanese accessions predominantly grouped into Uku Island and Fukue Island subclades. Within this population, we identified "G4-2" (JP248291) as the most salt tolerant, surpassing even the previously reported "Ukushima" accession. Both accessions collected from Uku Island, with accessions belonging to the Uku Island subclade exhibiting a strong trend of salt tolerance. Our results strongly suggest the occurrence of genetic mutations conferring enhanced salt tolerance in specific clade and region. This study highlights the potential of genetic analyses for identifying regions suitable for collecting valuable genetic resources for stress tolerance.